TWEAK/Fn14 pathway promotes a T helper 2-type chronic colitis with fibrosis in mice

Mucosal Immunology

Volumn 6, Issue 6, 2013, Pages 1131-1142

  Son, A ^a   Oshio, T ^a   Kawamura, Y I ^a   Hagiwara, T ^a   Yamazaki, M ^a   Inagaki Ohara, K ^a   Okada, T ^a   Wu, P ^b   Iseki, M ^a   Takaki, S ^a   Burkly, L C ^b   Dohi, T ^a  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HAPTEN; INTERLEUKIN 13; PROTEIN FN14; PROTEIN TWEAK; THYMIC STROMAL LYMPHOPOIETIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; COLITIS; COLON MUCOSA; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FIBROBLAST; INFLAMMATION; INTESTINAL FIBROSIS; KNOCKOUT MOUSE; LYMPHOCYTE PROLIFERATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TH2 CELL; WILD TYPE;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHRONIC DISEASE; COLITIS; COLON; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLASTS; FIBROSIS; HUMANS; IMMUNOGLOBULINS; INTERLEUKIN-13; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; RECEPTORS, CYTOKINE; RECEPTORS, TUMOR NECROSIS FACTOR; TH2 CELLS; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTORS;

EID: 84886029160     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2013.10     Document Type: Article

References (47)

1. Fichtner-Feigl, S., Strober, W., Geissler, E.K. & Schlitt, H.J. Cytokines mediating the induction of chronic colitis and colitis-Associated fibrosis. Mucosal immunol. 1 (Suppl 1), S24-S27 (2008).
2. Wynn, T.A. & Ramalingam, T.R. Mechanisms of fibrosis: Therapeutic translation for fibrotic disease. Nat Med. 18, 1028-1040 (2012).
3. Chicheportiche, Y. et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J. Biol. Chem. 272, 32401-32410 (1997).
4. Kaplan, M.J. et al. The apoptotic ligands TRAIL, TWEAK, and Fas ligand mediate monocyte death induced by autologous lupus Tcells. J. Immunol. 169, 6020-6029 (2002).
5. Maecker, H. et al. TWEAK attenuates the transition from innate to adaptive immunity. Cell 123, 931-944 (2005).
6. Nakayama, M. et al. Fibroblast growth factor-inducible 14 mediates multiple pathways of TWEAK-induced cell death. J. Immunol. 170, 341-348 (2003).
7. Justo, P. et al. Cytokine cooperation in renal tubular cell injury: The role of TWEAK. Kidney Int. 70, 1750-1758 (2006).
8. Burkly, L.C., Michaelson, J.S. & Zheng, T.S. TWEAK/Fn14 pathway: An immunological switch for shaping tissue responses. Immunol. Rev. 244, 99-114 (2011).
9. Winkles, J.A. The TWEAK-Fn14 cytokine-receptor axis: Discovery, biology and therapeutic targeting. Nat. Rev. Drug Discov. 7, 411-425 (2008).
10. Dohi, T. et al. TWEAK/Fn14 pathway: A nonredundant role in intestinal damage in mice through a TWEAK/intestinal epithelial cell axis. Gastroenterology 136, 912-923 (2009).
11. Kawashima, R. et al. Interleukin-13 damages intestinal mucosa via TWEAK and Fn14 in mice-A pathway associated with ulcerative colitis. Gastroenterology 141, 2119-2129 (2011).
12. Burkly, L.C. & Dohi, T. The TWEAK/Fn14 pathway in tissue remodeling: For better or for worse. Adv. Exp. Med. Biol. 691, 305-322 (2011).
13. Zheng, T.S. & Burkly, L.C. No end in site: TWEAK/Fn14 activation and autoimmunity associated- end-organ pathologies. J. Leukoc. Biol. 84, 338-347 (2008).
14. Perper, S.J. et al. TWEAK is a novel arthritogenic mediator. J. Immunol. 177, 2610-2620 (2006).
15. Kamata, K. et al. Involvement of TNF-like weak inducer of apoptosis in the pathogenesis of collagen-induced arthritis. J. Immunol. 177, 6433-6439 (2006).
16. Zhao, Z. et al. TWEAK/Fn14 interactions are instrumental in the pathogenesis of nephritis in the chronic graft-versus-host model of systemic lupus erythematosus. J. Immunol. 179, 7949-7958 (2007).
17. Wilson, M.S. & Wynn, T.A. Pulmonary fibrosis: Pathogenesis, etiology and regulation. Mucosal Immunol. 2, 103-121 (2009).
18. Ingram, J.L. et al. Opposing actions of Stat1 and Stat6 on IL-13-induced up-regulation of early growth response-1 and platelet-derived growth factor ligands in pulmonary fibroblasts. J. Immunol. 177, 4141-4148 (2006).
19. Fichtner-Feigl, S. et al. Induction of IL-13 triggers TGF-beta1-dependent tissue fibrosis in chronic 2,4,6-Trinitrobenzene sulfonic acid colitis. J. Immunol. 178, 5859-5870 (2007).
20. Wu, F. & Chakravarti, S. Differential expression of inflammatory and fibrogenic genes and their regulation by NF-kappaB inhibition in a mouse model of chronic colitis. J. Immunol. 179, 6988-7000 (2007).
21. Lawrance, I.C. et al. A murine model of chronic inflammation-induced intestinal fibrosis down-regulated by antisense NF-kappa B. Gastroenterology 125, 1750-1761 (2003).
22. Gordon, S. & Martinez, F.O. Alternative activation of macrophages: Mechanism and functions. Immunity 32, 593-604 (2010).
23. Pemberton, A.D. et al. Innate BALB/c enteric epithelial responses to Trichinella spiralis: Inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. J. Immunol. 173, 1894-1901 (2004).
24. Gu, N. et al. Intelectin is required for IL-13-inducedmonocyte chemotactic protein-1 and -3 expression in lung epithelial cells and promotes allergic airway inflammation. Am. J. Physiol. Lung. Cell. Mol. Physiol. 298, L290-L296 (2010).
25. Moro, K. et al. Innate production of T(H)2 cytokines by adipose tissue-Associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463, 540-544 (2010).
26. Neill, D.R. et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370 (2010).
27. Saenz, S.A. et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464, 1362-1366 (2010).
28. Bulek, K., Swaidani, S., Aronica, M. & Li, X. Epithelium: The interplay between innate and Th2 immunity. Immunol. Cell. Biol. 88, 257-268 (2010).
29. Saenz, S.A., Taylor, B.C. & Artis, D. Welcome to the neighborhood: Epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol. Rev. 226, 172-190 (2008).
30. Biton, M. et al. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat. Immunol. 12, 239-246 (2011).
31. Blazquez, A.B., Mayer, L. & Berin, M.C. Thymic stromal lymphopoietin is required for gastrointestinal allergy but not oral tolerance. Gastroenterology 139, 1301-1309 (2010).
32. He, R. et al. TSLP acts on infiltrating effector T cells to drive allergic skin inflammation. Proc. Natl. Acad. Sci. USA 105, 11875-11880 (2008).
33. Omori, M. & Ziegler, S. Induction of IL-4 expression in CD4(+) T cells by thymic stromal lymphopoietin. J. Immunol. 178, 1396-1404 (2007).
34. Allakhverdi, Z. et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J. Exp. Med. 204, 253-258 (2007).
35. Allakhverdi, Z., Smith, D.E.,Comeau,M.R. & Delespesse,G. Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J. Immunol. 179, 2051-2054 (2007).
36. Siracusa, M.C. et al. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature 477, 229-233 (2011).
37. Lee, H.C. & Ziegler, S.F. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkappaB. Proc. Natl. Acad. Sci. USA 104, 914-919 (2007).
38. Brown, S.A., Ghosh, A. & Winkles, J.A. Full-length, membraneanchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-kappaB pathway. J. Biol. Chem. 285, 17432-17441 (2010).
39. Roos, C. et al. Soluble and transmembrane TNF-like weak inducer of apoptosis differentially activate the classical and noncanonical NF-kappa B pathway. J. Immunol. 185, 1593-1605 (2010).
40. Tirnitz-Parker, J.E. et al. Tumor necrosis factor-like weak inducer of apoptosis is a mitogen for liver progenitor cells. Hepatology 52, 291-302 (2010).
41. Hotta, K. et al. Direct targeting of fibroblast growth factor-inducible 14 protein protects against renal ischemia reperfusion injury. Kidney Int. 79, 179-188 (2011).
42. Mittal, A. et al. The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J. Cell. Biol. 188, 833-849 (2010).
43. Jain, M. et al. A novel role for tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in the development of cardiac dysfunction and failure. Circulation 119, 2058-2068 (2009).
44. Hosokawa, Y., Hosokawa, I., Ozaki, K., Nakae, H. & Matsuo, T. Proinflammatory effects of tumour necrosis factor-like weak inducer of apoptosis (TWEAK) on human gingival fibroblasts. Clin. Exp. Immunol. 146, 540-549 (2006).
45. Meighan-Mantha, R.L. et al. The mitogen-inducible Fn14 gene encodes a type I transmembrane protein that modulates fibroblast adhesion and migration. J. Biol. Chem. 274, 33166-33176 (1999).
46. Jakubowski, A. et al. TWEAK induces liver progenitor cell proliferation. J. Clin. Invest. 115, 2330-2340 (2005).
47. Carpino, N. et al. Absence of an essential role for thymic stromal lymphopoietin receptor in murine B-cell development. Mol. Cell. Biol. 24, 2584-2592 (2004).